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Disease ecology

The silence of the robins

Nature volume 447, pages 652653 (07 June 2007) | Download Citation

A continent-wide analysis suggests that West Nile virus has severely affected bird populations associated with human habitats in North America. The declines parallel patterns of human disease caused by the virus.

Scenes reminiscent of those described in Rachel Carlson's Silent Spring1 have been occurring in suburban America. This time, it is not pesticides that are to blame for a decline in bird populations, but outbreaks of West Nile virus2. A study by LaDeau and colleagues3 on page 710 of this issue shows that reductions in bird populations correlate with the prevalence of the virus, that these patterns are upheld across years and throughout the continent, and that the patterns are geographically correlated with epidemics of human infection by West Nile virus*.

West Nile virus emerged in New York City from the Old World in 1999, and then spread rapidly across the entire continent. The primary hosts of the virus are birds, in which virus numbers are also amplified before the virus is transmitted by mosquitoes to the next victim. Besides birds, the virus can infect other vertebrates, including humans, and has caused the death of as many as 1,000 people4 in the United States alone, as well as uncounted casualties in birds and other vertebrates2,4 (Box 1).

Box 1: West Nile virus in the Old and New Worlds

West Nile virus was first isolated in 1937 in the West Nile province of Uganda10, an area known for other mosquito-transmitted diseases such as malaria, schistosomiasis, dengue and yellow fever. It has apparently only recently caused serious illness among humans11, and largely outside the tropics.

The first documented human epidemic occurred in Israel in 1951–54, with another in 1957. Major outbreaks occurred in South Africa (1974) and Israel (2000), with minor incidences in France (1962), Algeria (1994), Romania (1996) and Russia (1999), but only one in central Africa (1998).

Following its detection in the New World in 1999, West Nile virus spread quickly9 during the dry summer of 2002, and now occurs throughout North and Central America, and in the Caribbean4. It has killed individuals of almost 200 bird species in North America, as well as other wild and domestic animals2,4. By contrast, it seems that infected Old World birds rarely show adverse symptoms12.

The Old World human epidemics have generally been local and short-lived. But, as is the case with birds, the human effects of the virus in the New World are much more severe. Between 1999 and 2006, 23,974 cases were reported in the United States: 14,125 were of the mild West Nile fever, and 9,849 of the severe West Nile meningitis or encephalitis (inflammation of the spinal cord and brain), including 962 deaths4. There is currently no vaccine for humans.

The different effects of West Nile virus in the Old and New Worlds could be an example of host–parasite coevolution, in which the virus has coevolved with birds and humans in tropical Africa in particular, and so has a less lethal effect on its hosts12. If so, evolutionary adaptation might occur among New World species, which will minimize the virus's future impact.

Carsten Rahbek

LaDeau and colleagues have dealt with several analytical challenges to demonstrate that West Nile virus is indeed the main factor behind the observed large-scale declines in bird populations. Continent-wide fluctuations of this kind have been documented previously5,6, but they have been explained by changes in the local environment related to habitat, land use and climate. LaDeau and colleagues had to disentangle virus-induced mortality from these confounding effects.

To do so, they designed species-specific predictive models based on knowledge of the prevalence of the virus, exposure to mosquitoes and overall mortality for 20 different bird species, each species representing a specific combination of urban (human) association and susceptibility to the virus. The model was applied to 26 years of population data for six geographical regions to construct probability distributions for the expected abundance of each bird species in a given region before and after the arrival of the virus.

The results are revealing: significant population changes in seven of the 20 species were in agreement with specific expectations based on the direct adverse impact of virus infections. Although this may seem a modest effect, LaDeau and colleagues' analyses deliberately included tolerant bird species that were unlikely to be greatly affected for various ecological reasons. For the species thought to be susceptible to West Nile virus, there was a disturbingly consistent general relationship between the predicted effects of the virus and the observed declines in population abundance. The correlation was far from perfect. But it suggests that West Nile virus could potentially change the composition of bird communities across the entire continent.

Strikingly, the seven bird species that are most clearly affected by the virus are all 'peridomestic' — that is, they are associated with human populations, in this case those in town and city suburbs. Among the disappearing species is an icon of North American garden birds, the American robin (Turdus migratorius; Fig. 1). It is also thought-provoking that no fewer than 13 of the 20 species experienced a 10-year population low following the human epidemics of West Nile virus in 2002–03 in the United States3. This is a notable observation in light of the debate about the spread of the highly pathogenic avian influenza virus (H5N1 strain), and the potential role of migratory, peridomestic and domestic birds as reservoirs and dispersers of this disease.

Figure 1: Viral victim: the American robin.
Figure 1

Populations of this bird and of the American crow are among the seven species most clearly identified by LaDeau et al.3 as suffering from mortality caused by West Nile virus. The other five species for which there is a robust correlation between population declines and virus infection are the blue jay (Cyanocitta cristata), tufted titmouse (Baeolophus bicolor), house wren (Troglodytes aedon), chickadee (Poecile spp.) and Eastern bluebird (Sialia sialis). Image: R. NUSSBAUMER/NATUREPL.COM

LaDeau et al.3 caution against oversimplified interpretations of their results. The spatial patterns of disease that they detected may still reflect regional differences in the intensity of viral transmission, and these may be linked to spatial patterns in habitat, land use and climate — all of which are traditionally used to explain large-scale patterns of changes in bird populations.

The authors partly incorporated the potential influence of the El Niño/Southern Oscillation in their models as a crude measurement of climate variability, but their analysis does not include environmental or climatic parameters at the appropriate spatial scale. This may explain why, with the exception of the American crow (Corvus brachyrhynchos), the results are qualitatively rather inconsistent for individual species. But the results for the crow are compelling, not least given the geographical correlation with human infection shown in Figure 2 of the paper3.

More detailed analyses and studies on further species will be needed to fully understand the impact of West Nile virus on large-scale changes in North American bird populations. But even as it stands, this research reminds us once more of the threat of infectious diseases to both biodiversity and human health. The migratory passenger pigeon (Ectopistes migratorius) of North America, once the most abundant bird of its time with an estimated population of between 3 billion and 5 billion, was driven to extinction within a century by human agency and, possibly, diseases7. The disappearance of such an abundant species must have had a considerable effect on the communities in which it occurred. Indeed, it has been suggested that the rise in incidence of Lyme disease in humans is a delayed consequence of the removal of the passenger pigeon from the ecosystems of North America7,8.

We are witnessing the emergence of novel diseases at an unprecedented rate9. Epstein and colleagues9 have argued that human-induced changes in ecological systems and climate are now triggering “a barrage of emerging diseases that afflict humans, livestock, wildlife, marine organisms, and the very habitat we depend upon”. LaDeau and colleagues' study is a timely example of the effect that such diseases can have on communities of wild species and humans alike, even at a continental scale.

Notes

  1. 1.

    This article and the paper concerned3 were published online on 16 May 2007.

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  1. Carsten Rahbek is at the Center for Macroecology, Institute of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.  crahbek@.bi.ku.dk

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